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Mutualistic co-evolution of type III effector genes in Sinorhizobium fredii and Bradyrhizobium japonicum.

Kimbrel JA, Thomas WJ, Jiang Y, Creason AL, Thireault CA, Sachs JL, Chang JH - PLoS Pathog. (2013)

Bottom Line: We demonstrate that the rhizobial type III effector genes exhibit a surprisingly high degree of conservation in content and sequence that is in contrast to those of a well characterized plant pathogenic species.This type III effector gene conservation is particularly striking in the context of the relatively high genome-wide diversity of rhizobia.Instead, our results reveal that these loci are relatively static in rhizobial lineages and suggest that fitness conflicts between rhizobia mutualists and their host plants have been largely resolved.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America.

ABSTRACT
Two diametric paradigms have been proposed to model the molecular co-evolution of microbial mutualists and their eukaryotic hosts. In one, mutualist and host exhibit an antagonistic arms race and each partner evolves rapidly to maximize their own fitness from the interaction at potential expense of the other. In the opposing model, conflicts between mutualist and host are largely resolved and the interaction is characterized by evolutionary stasis. We tested these opposing frameworks in two lineages of mutualistic rhizobia, Sinorhizobium fredii and Bradyrhizobium japonicum. To examine genes demonstrably important for host-interactions we coupled the mining of genome sequences to a comprehensive functional screen for type III effector genes, which are necessary for many Gram-negative pathogens to infect their hosts. We demonstrate that the rhizobial type III effector genes exhibit a surprisingly high degree of conservation in content and sequence that is in contrast to those of a well characterized plant pathogenic species. This type III effector gene conservation is particularly striking in the context of the relatively high genome-wide diversity of rhizobia. The evolution of rhizobial type III effectors is inconsistent with the molecular arms race paradigm. Instead, our results reveal that these loci are relatively static in rhizobial lineages and suggest that fitness conflicts between rhizobia mutualists and their host plants have been largely resolved.

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T3E of S. fredii and B. japonicum have high levels of within-family amino acid identity.(A) Balloon plots of within-family amino acid conservation for translated T3Es. The percent amino acid identity was calculated for all pairwise comparisons within each family (y-axis) and plotted according to the number of members within families (x-axis). The sizes of the balloons are scaled with the largest representing 162 pairwise comparisons (the smallest balloons were enlarged). Unconfirmed T3E and pseudogene sequences were not included in the comparisons. (B) Kolmogorov–Smirnov test for all pairwise comparisons (connected by lines) of the distributions depicted in panel (A). Boxed p-values are significant (Bonferonni adjusted α level = 0.0083). (C) An F test for linear hypothesis was used to test for differences in percent amino acid identity for translated T3Es and core genes within each group. All p-values are significant (Bonferonni adjusted α level = 0.0125).
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ppat-1003204-g005: T3E of S. fredii and B. japonicum have high levels of within-family amino acid identity.(A) Balloon plots of within-family amino acid conservation for translated T3Es. The percent amino acid identity was calculated for all pairwise comparisons within each family (y-axis) and plotted according to the number of members within families (x-axis). The sizes of the balloons are scaled with the largest representing 162 pairwise comparisons (the smallest balloons were enlarged). Unconfirmed T3E and pseudogene sequences were not included in the comparisons. (B) Kolmogorov–Smirnov test for all pairwise comparisons (connected by lines) of the distributions depicted in panel (A). Boxed p-values are significant (Bonferonni adjusted α level = 0.0083). (C) An F test for linear hypothesis was used to test for differences in percent amino acid identity for translated T3Es and core genes within each group. All p-values are significant (Bonferonni adjusted α level = 0.0125).

Mentions: The sequences within T3E families of S. fredii and B. japonicum are also highly conserved, as more than 75% of the within-family pairwise comparisons had ≥90% amino acid identity (Figure 5A). Strikingly, twenty of the T3E families had all members with ≥99% identity. The T3Es of the group I P. syringae strains have a wider distribution in amino acid identity and a greater number of presence/absence polymorphisms than S. fredii or B. japonicum. Even when the latter variation was excluded from analysis, S. fredii and B. japonicum exhibit significantly more amino acid conservation of T3Es than group I P. syringae, whereas there was only marginal difference between the rhizobial lineages (Figure 5B).


Mutualistic co-evolution of type III effector genes in Sinorhizobium fredii and Bradyrhizobium japonicum.

Kimbrel JA, Thomas WJ, Jiang Y, Creason AL, Thireault CA, Sachs JL, Chang JH - PLoS Pathog. (2013)

T3E of S. fredii and B. japonicum have high levels of within-family amino acid identity.(A) Balloon plots of within-family amino acid conservation for translated T3Es. The percent amino acid identity was calculated for all pairwise comparisons within each family (y-axis) and plotted according to the number of members within families (x-axis). The sizes of the balloons are scaled with the largest representing 162 pairwise comparisons (the smallest balloons were enlarged). Unconfirmed T3E and pseudogene sequences were not included in the comparisons. (B) Kolmogorov–Smirnov test for all pairwise comparisons (connected by lines) of the distributions depicted in panel (A). Boxed p-values are significant (Bonferonni adjusted α level = 0.0083). (C) An F test for linear hypothesis was used to test for differences in percent amino acid identity for translated T3Es and core genes within each group. All p-values are significant (Bonferonni adjusted α level = 0.0125).
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3585131&req=5

ppat-1003204-g005: T3E of S. fredii and B. japonicum have high levels of within-family amino acid identity.(A) Balloon plots of within-family amino acid conservation for translated T3Es. The percent amino acid identity was calculated for all pairwise comparisons within each family (y-axis) and plotted according to the number of members within families (x-axis). The sizes of the balloons are scaled with the largest representing 162 pairwise comparisons (the smallest balloons were enlarged). Unconfirmed T3E and pseudogene sequences were not included in the comparisons. (B) Kolmogorov–Smirnov test for all pairwise comparisons (connected by lines) of the distributions depicted in panel (A). Boxed p-values are significant (Bonferonni adjusted α level = 0.0083). (C) An F test for linear hypothesis was used to test for differences in percent amino acid identity for translated T3Es and core genes within each group. All p-values are significant (Bonferonni adjusted α level = 0.0125).
Mentions: The sequences within T3E families of S. fredii and B. japonicum are also highly conserved, as more than 75% of the within-family pairwise comparisons had ≥90% amino acid identity (Figure 5A). Strikingly, twenty of the T3E families had all members with ≥99% identity. The T3Es of the group I P. syringae strains have a wider distribution in amino acid identity and a greater number of presence/absence polymorphisms than S. fredii or B. japonicum. Even when the latter variation was excluded from analysis, S. fredii and B. japonicum exhibit significantly more amino acid conservation of T3Es than group I P. syringae, whereas there was only marginal difference between the rhizobial lineages (Figure 5B).

Bottom Line: We demonstrate that the rhizobial type III effector genes exhibit a surprisingly high degree of conservation in content and sequence that is in contrast to those of a well characterized plant pathogenic species.This type III effector gene conservation is particularly striking in the context of the relatively high genome-wide diversity of rhizobia.Instead, our results reveal that these loci are relatively static in rhizobial lineages and suggest that fitness conflicts between rhizobia mutualists and their host plants have been largely resolved.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America.

ABSTRACT
Two diametric paradigms have been proposed to model the molecular co-evolution of microbial mutualists and their eukaryotic hosts. In one, mutualist and host exhibit an antagonistic arms race and each partner evolves rapidly to maximize their own fitness from the interaction at potential expense of the other. In the opposing model, conflicts between mutualist and host are largely resolved and the interaction is characterized by evolutionary stasis. We tested these opposing frameworks in two lineages of mutualistic rhizobia, Sinorhizobium fredii and Bradyrhizobium japonicum. To examine genes demonstrably important for host-interactions we coupled the mining of genome sequences to a comprehensive functional screen for type III effector genes, which are necessary for many Gram-negative pathogens to infect their hosts. We demonstrate that the rhizobial type III effector genes exhibit a surprisingly high degree of conservation in content and sequence that is in contrast to those of a well characterized plant pathogenic species. This type III effector gene conservation is particularly striking in the context of the relatively high genome-wide diversity of rhizobia. The evolution of rhizobial type III effectors is inconsistent with the molecular arms race paradigm. Instead, our results reveal that these loci are relatively static in rhizobial lineages and suggest that fitness conflicts between rhizobia mutualists and their host plants have been largely resolved.

Show MeSH
Related in: MedlinePlus